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Interneuron-specific plasticity at parvalbumin and somatostatin inhibitory synapses onto CA1 pyramidal neurons shapes hippocampal output

Author

Listed:
  • Matt Udakis

    (University of Bristol)

  • Victor Pedrosa

    (Imperial College London)

  • Sophie E. L. Chamberlain

    (University of Bristol)

  • Claudia Clopath

    (Imperial College London)

  • Jack R. Mellor

    (University of Bristol)

Abstract

The formation and maintenance of spatial representations within hippocampal cell assemblies is strongly dictated by patterns of inhibition from diverse interneuron populations. Although it is known that inhibitory synaptic strength is malleable, induction of long-term plasticity at distinct inhibitory synapses and its regulation of hippocampal network activity is not well understood. Here, we show that inhibitory synapses from parvalbumin and somatostatin expressing interneurons undergo long-term depression and potentiation respectively (PV-iLTD and SST-iLTP) during physiological activity patterns. Both forms of plasticity rely on T-type calcium channel activation to confer synapse specificity but otherwise employ distinct mechanisms. Since parvalbumin and somatostatin interneurons preferentially target perisomatic and distal dendritic regions respectively of CA1 pyramidal cells, PV-iLTD and SST-iLTP coordinate a reprioritisation of excitatory inputs from entorhinal cortex and CA3. Furthermore, circuit-level modelling reveals that PV-iLTD and SST-iLTP cooperate to stabilise place cells while facilitating representation of multiple unique environments within the hippocampal network.

Suggested Citation

  • Matt Udakis & Victor Pedrosa & Sophie E. L. Chamberlain & Claudia Clopath & Jack R. Mellor, 2020. "Interneuron-specific plasticity at parvalbumin and somatostatin inhibitory synapses onto CA1 pyramidal neurons shapes hippocampal output," Nature Communications, Nature, vol. 11(1), pages 1-17, December.
  • Handle: RePEc:nat:natcom:v:11:y:2020:i:1:d:10.1038_s41467-020-18074-8
    DOI: 10.1038/s41467-020-18074-8
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    Cited by:

    1. Li, Xuening & Xie, Ying & Ye, Zhiqiu & Huang, Weifang & Yang, Lijian & Zhan, Xuan & Jia, Ya, 2024. "Chimera-like state in the bistable excitatory-inhibitory cortical neuronal network," Chaos, Solitons & Fractals, Elsevier, vol. 180(C).
    2. Ruy Gómez-Ocádiz & Massimiliano Trippa & Chun-Lei Zhang & Lorenzo Posani & Simona Cocco & Rémi Monasson & Christoph Schmidt-Hieber, 2022. "A synaptic signal for novelty processing in the hippocampus," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    3. Jan C. Frankowski & Alexa Tierno & Shreya Pavani & Quincy Cao & David C. Lyon & Robert F. Hunt, 2022. "Brain-wide reconstruction of inhibitory circuits after traumatic brain injury," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    4. Giulia Faini & Dimitrii Tanese & Clément Molinier & Cécile Telliez & Massilia Hamdani & Francois Blot & Christophe Tourain & Vincent Sars & Filippo Bene & Benoît C. Forget & Emiliano Ronzitti & Valent, 2023. "Ultrafast light targeting for high-throughput precise control of neuronal networks," Nature Communications, Nature, vol. 14(1), pages 1-18, December.

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